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Non-invasive multi-species monitoring: real-time PCR detection of small mammal and squirrel prey DNA in pine marten (Martes martes) scats

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Abstract

DNA identification of mammal species occurring in the diet of a predator is potentially a useful approach to remotely monitor the distribution of multiple species. This is important in Ireland, where it has been shown that the combined presence of the introduced bank vole and greater white-toothed shrew impact the distribution of the indigenous small mammals, the wood mouse and pygmy shrew. Direct monitoring of these species and their interactions requires trap**, a labour-intensive and costly approach. In this study, we applied an indirect method by genetically testing the presence of small mammals in pine marten scats collected during the National Pine Marten Survey (2005–2007) to map their distribution. We also included additional scats to investigate if less common prey items, the red squirrel and grey squirrel, could also be detected. This study demonstrates that all target species were genetically detected from pine marten scats. This strategy could be implemented as a monitoring programme for indigenous and introduced mammal species.

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References

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Balestrieri A, Remonti L, Ruiz-González A, Vergara M, Capelli E, Gómez-Moliner B, Prigioni C (2011) Food habits of genetically identified pine marten (Martes martes) expanding in agricultural lowlands (NW Italy). Acta Theriol 56:199–207

    Google Scholar 

  • Baltrūnaitė L (2002) Diet composition of the red fox (Vulpes vulpes L.), pine marten (Martes martes L.) and raccoon dog (Nyctereutes procyonoides Gray) in clay plain landscape, Lithuania. Acta Zool. Lituanica 4:362–368

    Article  Google Scholar 

  • Bowles E, Schulte PM, Tollit DJ, Deagle BE, Trites AW (2011) Proportion of prey consumed can be determined from faecal DNA using real-time PCR. Mol Ecol Resour 11:530–40

    Google Scholar 

  • Brändli L, Lawson Handley L, Vogel P, Perrin N (2005) Evolutionary history of the greater white-toothed shrew (Crocidura russula) inferred from analysis of mtDNA, Y, and X chromosome markers. Mol Phylo and Evol 37:832–44

    Article  Google Scholar 

  • Carey M, Hamilton G, Poole A, Lawton C (2007) The Irish squirrel survey 2007. COFORD, Dublin

    Google Scholar 

  • Caryl FM, Raynor R, Quine CP, Park KJ (2012) The seasonal diet of British pine marten determined from genetically identified scats. J Zool 288:52–259

    Article  Google Scholar 

  • de Marinis AM, Marsseti M (1995) Feeding habits of the pine marten Martes martes L., 1758, in Europe: a review. Hystrix 7:143–150

    Google Scholar 

  • Deagle BE, Tollit DJ, Jarman SN, Hindell MA, Trites AW, Gales NJ (2005) Molecular scatology as a tool to study diet: analysis of prey DNA in scats from captive Steller sea lions. Mol Ecol 14:1831–42

    Article  CAS  PubMed  Google Scholar 

  • Dooley JJ, Paine KE, Garrett SD, Brown HM (2004) Detection of meat species using TaqMan real-time PCR assays. Meat Sci 68:431–438

    Article  CAS  PubMed  Google Scholar 

  • Helldin JO (1999) Diet, body condition, and reproduction of Eurasian pine martens Martes martes during cycles in microtine density. Ecography 22:324–336

    Article  Google Scholar 

  • Helldin JO (2000) Seasonal diet of pine marten Martes martes in southern boreal Sweden. Acta Theriol 45:409–420

    Google Scholar 

  • Krauze-Gryz D, Gryz J, Goszczyński J (2012) Predation by domestic cats in rural areas of central Poland: an assessment based on two methods. J Zool 288:260–266

    Article  Google Scholar 

  • Lynch AB, McCann Y (2007) The diet of the pine marten (Martes martes) in Killarney National Park. Biol Environ Proc R Ir Acad 107:67–76

    Article  Google Scholar 

  • Matejusová I, Doig F, Middlemas SJ, Mackay S, Douglas A, Armstrong JD, Cunningham CO, Snow M (2008) Using quantitative real-time PCR to detect salmonid prey in scats of grey (Halichoerus grypus) and harbour (Phoca vituline) seals in Scotland: an experimental and field study. J Appl Ecol 45:632–640

    Article  Google Scholar 

  • McDevitt AD, Rambau RV, O′Brien J, McDevitt CD, Hayden T, Searle JB (2009) Genetic variation in Irish pygmy shrews Sorex minutus (Soricomorpha: Soricidae): implications for colonization history. Biol J Linn Soc 97:918–927

    Article  Google Scholar 

  • Montgomery WI, Lundy MG, Reid N (2012) “Invasional meltdown”: evidence for unexpected consequences and cumulative impacts of multispecies invasions. Biol Invasions 6:111–1125

    Google Scholar 

  • Moran S, Turner PD, O′Reilly C (2008) Non-invasive genetic identification of small mammal species using real-time polymerase chain reaction. Mol Ecol Res 8:1267–1269

    Article  CAS  Google Scholar 

  • Mullins J, Statham MJ, Roche T, Turner PD, O′Reilly C (2010) Remotely plucked hair genoty**: a reliable and non-invasive method for censusing pine marten (Martes martes, L. 1758) populations. Eur J Wildl Res 56:443–453

    Article  Google Scholar 

  • Murray DC, Bunce M, Cannell BL, Oliver R, Houston J, White NE, Barrero RA, Bellgard MI, Haile J (2011) DNA-based faecal dietary analysis: a comparison of qPCR and high throughput sequencing approaches. PLoS One 6:e25776

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • O'Mahony D, Turner P, O'Reilly C (2012) Pine marten (Martes martes) distribution and abundance in Ireland: a cross-jurisdictional analysis using non-invasive genetic survey techniques. Mamm Biol 77:351–357

    Google Scholar 

  • O'Meara DB, Turner PD, Coffey L, O'Reilly C (2012) TaqMan assays for species identification of the red squirrel (Sciurus vulgaris) and the grey squirrel (Sciurus carolinensis). Conserv Genet Res 4:603–604

    Article  Google Scholar 

  • O'Reilly C, Statham M, Mullins J, Turner PD, O'Mahony D (2008) Efficient species identification of pine marten (Martes martes) and red fox (Vulpes vulpes) scats using a 5′ nuclease real-time PCR assay. Conserv Genet 9:735–73

    Article  Google Scholar 

  • O'Teangana D, Reilly S, Montgomery WI, Rochford J (2000) Distribution and status of the red squirrel (Sciurus vulgaris) and grey squirrel (Sciurus carolinensis) in Ireland. Mammal Rev 30:45–56

    Article  Google Scholar 

  • Rosellini S, Barj PA (2008) The response of European pine marten (Martes martes L.) feeding to the changes of small mammal abundance. Pol J Ecol 56:497–504

    Google Scholar 

  • Ruiz-González A, Rubines J, Berdión O, Gómez-Moliner BJ (2007) A non-invasive genetic method to identify the sympatric mustelids pine marten (Martes martes) and stone marten (Martes foina): preliminary distribution survey on the northern Iberian Peninsula. Eur J Wildl Res 54:253–261

    Article  Google Scholar 

  • Searle JB (2008) The colonization of Ireland by mammals. In: Davenport JL, Sleeman DP, Woodman PC (eds) Mind the gap: postglacial colonization of Ireland. Irish Nat J Special Supplement: 109–115.

  • Shehzad W, Riaz T, Nawaz MA, Miquel C, Poillot C, Shah SA, Pompanon F, Coissac E, Taberlet P (2012) Carnivore diet analysis based on next-generation sequencing: application to the leopard cat (Prionailurus bengalensis) in Pakistan. Mol Ecol 8:1951–1965

    Article  Google Scholar 

  • Stuart P, Mirimin L, Cross TF, Sleeman DP, Buckley NJ, Telfer S, Birtles RJ, Kotlik P, Searle JB (2007) The origin of Irish bank voles (Clethrionomys glareolus) assessed by mitochondrial DNA analysis. Irish Nat J 28:440–446

    Google Scholar 

  • Tosh DG, Lusby J, Montgomery I, O'Halloran J (2008) First record of greater white-toothed shrew Crocidura russula in Ireland. Mamm Rev 38:321–326

    Article  Google Scholar 

  • Warner P, O'Sullivan P (1982) The food of the pine marten (Martes martes) in Co. Clare. Trans Intern Congr Game Biol 14:323–330

    Google Scholar 

  • Yalden DW (1999) The history of British mammals. Poyser, London

    Google Scholar 

  • Zalewski A (2004) Geographical and seasonal variation in food habits and prey size of the European pine martens. In: Harrison DJ, Fuller AK (eds) Martens and fishers (Martes) in human-altered environments: an international perspective. Springer, New York, pp 77–98

    Google Scholar 

  • Zarzoso-Lacoste D, Corse E, Vidal E (2013) Improving PCR detection of prey in molecular diet studies: importance of group specific primer set selection and extraction protocol performances. Mole Ecol Res 13:117–127

    Google Scholar 

  • Zhou YB, Newman C, Xu WT, Buesching CD, Zalewski A, Kaneko Y, Macdonald DW, **e ZQ (2011) Biogeographical variation in the diet of holarctic martens (genus Martes, mammalia: Carnivora: Mustelidae): adaptive foraging in generalists. J Biogeogr 38:137–147

    Article  Google Scholar 

Download references

Acknowledgments

The MISE project is partly funded by the European Development Fund funded by INTERREG IVA (2007–2013). DOM and ES were supported by the EMBARK Strand 1 Initiative and the Irish Research Council for Science, Engineering and Technology (IRCSET), respectively. We would like to thank the associate editor, Allan McDevitt, anonymous reviewers and Jacinta Mullins for their constructive comments to help improve the manuscript.

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Authors and Affiliations

  1. Molecular Ecology Research Group, Waterford Institute of Technology, Cork Road, Waterford, Ireland

    Denise B. O’Meara, Peter D. Turner & Catherine O’Reilly

  2. Mammal Ecology Group, School of Natural Sciences, Ryan Institute, National University of Ireland, Galway, Ireland

    Emma Sheehy & Colin Lawton

  3. Ecological Management Group, Ormeau Business Park, Belfast, BT7 2JA, Northern Ireland, UK

    Declan O’Mahony

  4. Mammals in a Sustainable Environment (MISE) Project, Waterford County Council, Tramore Civic Offices, Tramore, Co., Waterford, Ireland

    Andrew P. Harrington

  5. Selectfor, Brechfa, Carmarthenshire, Wales, UK

    Huw Denman

  6. MISE Project, The Vincent Wildlife Trust, Brechfa, Carmarthenshire, Wales, UK

    Jenny MacPherson

Authors
  1. Denise B. O’Meara
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  2. Emma Sheehy
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  3. Peter D. Turner
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  4. Declan O’Mahony
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  5. Andrew P. Harrington
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  6. Huw Denman
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  7. Colin Lawton
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  8. Jenny MacPherson
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  9. Catherine O’Reilly
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Corresponding author

Correspondence to Denise B. O’Meara.

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Communicated by: Cino Pertoldi

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O’Meara, D.B., Sheehy, E., Turner, P.D. et al. Non-invasive multi-species monitoring: real-time PCR detection of small mammal and squirrel prey DNA in pine marten (Martes martes) scats. Acta Theriol 59, 111–117 (2014). https://doi.org/10.1007/s13364-013-0155-8

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  • DOI: https://doi.org/10.1007/s13364-013-0155-8

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